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Graded Potentials and Spiking in Single Units of the Oval Organ, a Mechanoreceptor in the Lobster Ventilatory System Ii

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Graded Potentials and Spiking in Single Units of the Oval Organ, a Mechanoreceptor in the Lobster Ventilatory System Ii J. exp. Biol. 107, 451-464 (1983) 45 \ Printed in Great Britain © The Company of Biologists Limited 1983 GRADED POTENTIALS AND SPIKING IN SINGLE UNITS OF THE OVAL ORGAN, A MECHANORECEPTOR IN THE LOBSTER VENTILATORY SYSTEM II. INDIVIDUALITY OF THE THREE AFFERENT FIBRES BYB. M. H. BUSH Department of Physiology, University of Bristol, Park Row, Bristol BS15LS AND V. M. PASZTOR Department of Biology, McGill University, 1205 Avenue Dr. Penfield, Montreal, Canada H3A 1B1 {Received 14 March 1983-Accepted 24 June 1983) SUMMARY 1. The peripheral dendritic arborizations of sensory units X, Y and Z of the oval organ have similar branching patterns. All three permeate the whole array of connective tissue strands without apparent regionalization or specialization. 2. The analogue components of sensory responses elicited in fibres X, Y and Z when the connective tissue array is stretched show considerable diver- sity: fibre Z has a higher threshold than X and Y; the dynamic peak values of X and Y saturate at pulls mid-range for Z; X, Y and Z form a spectrum of increasing adaptation. 3. Application of TTX abolishes impulse generation in fibre X earlier than in fibre Y, indicating diversity in spike initiating mechanisms from one fibre type to another. 4. Fibre X only spikes between certain limits of membrane depolariza- tion. Usually the response includes one to five spikes which occur during the dynamic phase of a trapezoidal stretch stimulus. 5. Fibre Y fires throughout the stimulus duration for pulls of moderate amplitude and velocity. Spiking inactivation and a low maximum firing frequency (approximately 80s"') limit the range of length sensitivity in fibre Y. 6. Fibre Z attains higher firing frequencies than either X or Y (approximately 110 s"1). The initial burst frequency (velocity dependent) may equal the firing rate of the dynamic peak. INTRODUCTION In the preceding paper (Pasztor & Bush, 1983) we have shown that each of three sensory afferents of the oval organ is capable of transmitting both graded potentials Key words: Mechanoreceptor, receptor potentials, impulse patterns, Crustacea. 452 B. M. H. BUSH AND V. M. PASZTOR and spikes. Thus each fibre has available two methods of information transfer, effec- tively doubling the number of information channels. Since the oval organ is the onl)| proprioceptor which has so far been identified in the second maxilla as being capable of providing sensory feedback about respiratory beating (Pasztor, 1969), any increase in signalling capacity is likely to be of significance to the animal. In this paper we investigate the differences which exist between the sensory res- ponses recorded from oval organ afferents X, Y and Z. We will show that the com- pound response of each fibre has distinctive characteristics which are consistent from one preparation to another. This analysis forms the basis for a current study on the functional role of the oval organ in the control of gill ventilation. MATERIALS AND METHODS An isolated preparation of the oval organ was dissected from the second maxilla of Homarus as described in the preceding paper (Pasztor & Bush, 1983). The oval base of cuticle was anchored to the Sylgard lining of the bath, while the apex of the organ was attached to the puller assembly by which stretch stimuli were presented. Standard trapezoidal (ramp-and-hold) stimuli were presented to the organ at 1-min intervals. Pull amplitude, ramp duration and total stimulus duration were controlled by a function generator. During series of graded amplitude stimuli, ramp duration was held constant and, as a consequence, ramp velocity increased concurrently with amplitude. Intracellular recordings were taken from pairs of 3 M-KCl-filled micropipettes (15-25 Mfi) inserted into adjacent afferents as close together as possible. Responses were recorded on-line or stored on tape for subsequent analysis, using an Apple-Isaac microprocessor system. RESULTS Distribution of sensory terminals In a previous paper (Pasztor, 1979) the sensory dendrites of the oval organ arboriza- tion were shown to end in naked bulbous terminals, anchored between epidermal cells at the base of an array of connective tissue strands. That ultrastructural study sugges- ted that the terminals of all three fibres, X, Y and Z, formed a single population indistinguishable from one another, and that each fibre gave rise to branches distributed throughout the whole oval organ. Cobalt backfills of the sensory arborization, through the cut distal stump of the scaphognathite nerve, have confirmed the pervasive nature of dendritic branching. The photograph of one such backfill, Fig. 1, shows closely similar (though not identi- cal) branching of primary dendrites in two stained sensory units. Both penetrate all parts of the oval, and give rise to an even distribution of terminal branches. There is no indication of regionalization or specialization of the arborization of any one fibre. Differences between X, Y and Z responses attributable to the receptor potential The graded potentials of X, Y and Z fibres exhibited great diversity in waveform and amplitude (Figs 2,3). Fig. 4 plots potential magnitude versus stimulus amplitude Journal of Experimental Biology, Vol. 107 Fig. 1 mn Fig. 1. Sensory arborization of the oval organ. Dorsal view of-cobalt backfill through arthrodia] membrane at insertion of connective tissue strands. Two sensory units (sn I and sn2) distribute throughout the oval with very similar branching pattern. Motor axons (mn I and mn2) in the same nerve trunk continue straight through the oval organ. Scale bar= 100/mi. M. H. BUSH AND V. M. PASZTOR (Facing p. 452) Characteristics of oval organ afferent fibres 453 0-175 mm 0-2 0-25 0-3 25 mV 0-35 0-45 0-55 Is Fig. 2. Comparison of X and Y fibre responses recorded concurrently during a series of trapezoidal pulls of increasing amplitude (as indicated). Ramp duration, 140 ms; total pull, 1-0 s. Recording sites 55 mm from confluence of oval organ dendrites. 0-3 mm 0-5 25 mV Is Fig. 3. Comparison of X and Z fibre responses recorded concurrently during a series of pulls of increasing amplitude. Stimulus parameters as in Fig. 2. Recording sites 5'5 mm from oval organ. for representative X, Y and Z fibres. The peak dynamic and adapted static values were estimated, in the spiking responses of fibres Y and Z, from lines connecting the troughs of the post-spike afterpotentials. These are underestimates, which may displace the curves downwards, but we think they give an acceptable representation of the shape of the graded potentials, since they are comparable with data from tetrodotoxin-treated fibres (see Fig. 5). In the examples shown here in Fig. 4, X and 454 B. M. H. BUSH AND V. M. PASZTOR 01 0-4 0-5 0-6 Pull amplitude (mm) Fig. 4. Relationship between graded potential amplitude and pull amplitude for representative X, Y and Z fibre*. X and Y recorded concurrently. Z values taken from another, matched, preparation. Closed symbols: dynamic peak values. Open symbols: static, adapted levels. Recording sites 5-5 mm from oval organ. Stimulus parameters as in Fig. 2. Y responses were recorded concurrently. The Z responses were from an X-Z pair of a different preparation, chosen because the X responses (not shown) matched in threshold and amplitude the X data used in the graph. This ensures that the two preparations were undergoing comparable stimulation. Three factors emerge from analysis of these and other similar examples. Firstly, fibre Z has a higher threshold to small stretch stimuli than X and Y. Both X and Y can discriminate between small increments of stretch with proportionate increases in graded potential amplitude, within the low part of the stimulus range, which is around threshold for Z (see Figs 3 and 12). Secondly, the dynamic peak values of X and Y saturate at mid-range pulls, leaving Z to encode length information at the upper end of the useful range of the whole organ. Thirdly, by comparing the dynamic and static curves for each fibre, it can be seen that the extent of graded potential adaptation differs significantly between fibres. There is minimal adaptation in X, moderate in Y and maximal in Z. Nakajima & Onodera (1969) found only slight generator potential adaptation in the paired crayfish MRO units, and ascribed their distinctive phasic and tonic firing patterns to differences in impulse initiation. This is not altogether the case with the oval organ as is clearly shown in responses of tetrodotoxin-treated fibres (Figs 5, 6). Once all spiking is abolished, the remaining graded potential in fibre Y (and Z, not illustrated) shows a distinct adaptive decline during the static phase of stretch, and Characteristics of oval organ afferent fibres 455 JllUl 1-5 TTX 2-5 3-5 25 mV Fig. 5. Differential time course of spike abolition by tetrodotoxin (TTX) in X and Y fibres. Samples from a series of responses recorded at 1-min intervals. Times of exposure to 8 X 10"7M-TTX are indicated. Concurrent recordings; upper: fibre X; lower: fibre Y. 25 mV O'l mm 0-2 Is Fig. 6. Comparison of X and Y fibre responses to series of pulls of increasing amplitude after spike abolition with tetrodotoxin. Note the similar dynamic peaks of the two, but more pronounced adapta- tion in fibre Y. this is reflected in the spike adaptation prior to tetrodotoxin (TTX) application. In contrast fibre X shows almost no receptor potential adaptation after TTX treatment. This in turn suggests that the initial transient peak in the graded potential underlying 456 B. M. H. BUSH AND V. M. PASZTOR the brief burst of spikes in X may be a property of the spike generating neural membrane (see below).
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